in the recovery of iron mining areas in Minas Gerais, Brazil
Garcia, LC.
a,b, Barros, FV.
band Lemos-Filho, JP.
b*
aLaboratório de Ecologia e Restauração Florestal,
Escola Superior de Agricultura “Luiz de Queiroz” – ESALQ, Universidade de São Paulo – USP, Av. Pádua Dias, 11, CP 9, CEP 13418-900, Piracicaba, SP, Brazil
bLaboratório de Fisiologia Vegetal,Departamento de Botânica – Instituto de Ciências Biológicas,
Universidade Federal de Minas Gerais – UFMG,
Av. Antônio Carlos, 6627, CEP 31270-110, Belo Horizonte, MG, Brazil *e-mail: lemos@icb.ufmg.br
Received November 12, 2007 – Accepted March 6, 2008 – Distributed August 31, 2009 (With 4 figures)
Abstract
“Canga” is a name given to the ferruginous rocky fields that can be found in the “Quadrilátero Ferrífero” of Minas Gerais, Brazil. The endemism and species richness make them areas of special biological importance, regarded as high-priority for conservation. Nevertheless, they are being threatened by intense mining activity. Aiming to under-stand more about this flora, this study was performed in order to determine the maturation or dispersal period of the fruits of four Canga species, Alibertia vaccinioides K.Schum. (Rubiaceae), Coccoloba acrostichoides Cham. (Polygonaceae), Miconia sellowiana Naudin (Melastomataceae), and one probable new species of Calyptranthes Sw. (Myrtaceae). Although fruit maturation or dispersal tended to occur at the end of the dry season, some asynchrony was observed in these species, with food sources being available during most of the year. This shows that these species have the potential to attract animals the whole year round, and planting them for the recovery of iron mining areas may increase the community’s self-regeneration capacity, leading to a more successful restoration process.
Keywords: fleshy fruit, ironstone outcrop, rocky field, seasonality, zoochoric species.
Fenologia da frutificação como importante ferramenta na recuperação
de áreas de mineração de ferro em Minas Gerais, Brasil
Resumo
Canga é um nome dado para os campos rupestres ferruginosos encontrados no Quadrilátero Ferrífero de Minas Gerais. O endemismo e riqueza de espécies os tornam uma área de importância biológica especial, considerada prioritária para conservação. Além disso, tem sido submetida à intensa atividade mineradora. Este estudo objetivou determinar as épocas de maturação/dispersão de frutos de quatro espécies de ocorrência na canga, Alibertia vaccinioides K. Schum. (Rubiaceae), Coccoloba acrostichoides Cham. (Polygonaceae), Miconia sellowiana Naudin (Melastomataceae) e de uma provável espécie nova de Calyptranthes Sw. (Myrtaceae). Apesar da maturação/dispersão dos frutos ter apre-sentado uma tendência de ocorrer no final da estação seca, foi constatada uma assincronia do evento entre essas espécies, com disponibilidade de alimento aos animais frugívoros ao longo de grande parte do ano. O plantio dessas espécies para recuperação de áreas ferruginosas similares degradadas pela mineração poderá atrair fauna durante todas as estações, aumentando o potencial de autorregeneração da comunidade e o consequente sucesso no processo de restauração.
Palavras-chave: afloramentos rochosos, campos rupestres, espécies zoocóricas, frutos carnosos, sazonalidade.
1. Introduction
The “Quadrilátero Ferrífero” (Ferriferous Quadrilateral) region is regarded as a conservation prior-ity area with special biological importance that demands urgent scientific investigation, due to its plant and am-phibian endemisms, richness of vertebrate species, and
tifying their relative contribution to fruit availability to local fauna.
2. Materials and Methods
This study was conducted in an area covered by an ironstone outcrop vegetation called “Canga couraçada” (armor-clad “Canga”) (Rizzini, 1979), which has a heter-ogeneous flora (Oliveira and Stehmann, 2007). It is situ-ated near the county of Barão de Cocais (19° 53’ 08” S and 43° 26’ 11” W), in the Quadrilátero Ferrífero of Minas Gerais, southeastern Brazil (Figure 1), at an alti-tude of 1,120 m. The wet season occurs from November to March, and the dry season from April to August, when rainfall is less than 20 mm/month. The “Canga’s” heat-ing durheat-ing the day, and its fast coolheat-ing at night result in a broad range of daily temperatures (Vincent et al., 2002), an important characteristic of this area.
A floristic study identified 117 species, with pre-dominance of shrubs and herbaceous species (Oliveira and Stehmann, 2007). Four of these species were studied in this work, namely: Alibertia vaccinioides
K.Schum. (Rubiaceae), Coccoloba acrostichoides
Cham. (Polygonaceae), both restricted to the state of Minas Gerais (Melo, 2000); a probable new species of
Calyptranthes Sw. (Myrtaceae) (Sobral, pers. comm.), and Miconia sellowiana Naudin (Melastomataceae). According to characteristics described by Van der Pijl (1982), these species present zoochoric dispersal syn-drome, and they were chosen because they were the pre-vailing zoochoric species found in the area during initial visits. Except for M. sellowiana, which is a tree, these are shrub species. The botanical material collected was included in the herbarium collection of the Department of Botany at the Federal University of Minas Gerais (BHCB). Visits were performed monthly during a period of 15 months. During each visit, the maturation or dis-persal of fruits of ten previously marked individuals of each species was observed in the field. Fruit maturation was characterised by changes in fruit colour and disper-sal was defined as the falling of fruits. The species’ be-haviour was described using the index of activity based on phenophase presence or absence, as per Bencke and Morellato (2002).
Circular data analysis, using the ORIANA software (Kovach, 2002), was performed in order to verify the lev-el of synchrony among individuals disposed around an average angle, which means the average date on which the phenophase occurs with the highest frequency. Based on the dates of field visits, the test generates an average vector (µ), its significance (Rayleigh test p), and an aver-age vector length (r). The averaver-age vector (µ), represented in degrees, allows one to calculate the average date on which there is a high probability of finding individuals of each species in a certain phenophase. The average vec-tor’s significance (Rayleigh test p) points out the prob-ability of the data being randomly distributed around the circle of 360°. Average vector length (r) is an index that large mineral reserves. In Brazil, the two most important
reserves are “Serra de Carajás” (Carajás Mountains), in the Amazon forest, and the Quadrilátero Ferrífero, in the southeast. Brazil is the world’s second largest iron ore producer, and about 75% of this production is extracted from the Quadrilátero Ferrífero, where, currently, about 50 opencast mines are in activity (Jacobi et al., 2007). Therefore, this environment has been suffering expres-sive impact from the extraction of iron ore, and that is why special attention to its conservation and recupera-tion is required.
Mining is one of the main activities that cause dras-tic changes in landscape (Frenedozo, 2004) and impacts on wildlife. Rehabilitation programs for these areas are sometimes difficult to implement, for there are some gaps in the knowledge about the “canga” environment. The first approaches used non-native species, but ef-forts have been proposed towards inserting native spe-cies during this process (Parrotta and Knowles, 1999; Grant, 2006). However, the use of native species is only possible with previous knowledge about their biology, such as population dynamics, phenology, reproductive success, seed germination, seedling establishment, and growth rate. Therefore, studies that investigate the bi-ology of native species are of great importance to their management and to the restoration of degraded areas. Phenological studies, which may be applied to the re-generation of forests (Parrado-Rosselli, 2006), help to understand plant-animal interactions, the communities’ resource availability through time, and the evolution of the life history of animals that depend on plants for feed-ing (Frenedozo, 2004).
The fitness of individuals within isolated plant popu-lations, such as those of mountaintop “Cangas”, depends on successful dispersal among populations, as do the creation and maintenance of metapopulations and the necessary species migrations in response to environmen-tal changes (Martine et al., 2004). Hence, the phenology of fruiting has an important bearing on community di-versity, as frugivorous species depend on a constant food supply (Fenner, 1998) and some plant species depend on animals for their dispersal. The competition for dispers-ers can result in a pattern of responses for the purpose of reducing phenological overlapping among species, resulting in asynchronous ripening periods (Van Schaik et al., 1993).
iden-ranges from 0, or complete asynchrony of the event, to 1, which represents the highest possible synchrony (Zar, 1996).
The circular analysis was applied to the fruit disper-sal or maturation of each species separately, in order to verify interspecific variations. The test was also applied to all individuals, without distinction of species, during the first year of study (September/2002 – August/2003), in order to verify the phenological synchrony of this event at the community level.
3. Results
The species showed different maturation or dis-persal behaviours (Figures 2 and 3). The fruits of
Alibertia vaccinioides matured and/or were dispersed over many months, with only a few individuals provid-ing food resources to frugivorous animals each month.
Calyptranthes sp. was the only species that offered fruits in October/2002 and August/2003. This species was the main food provider, with a high number of individuals
Figure 1. Study area, “Brucutu’s Mine” in Minas Gerais State, southeast Brazil. Below, map of the Quadrilátero Ferrífero,
bearing ripe fruits. The species that presented the shortest resource availability period (two months) was Miconia sellowiana. Conversely, Coccoloba acrostichoides dis-played the largest continuous period of ripe fruit avail-ability (seven months), and was the only species that of-fered resources in May/2003. The highest limitation of resources to frugivorous animals by part of the studied species occurred in November/2002 and 2003 and in March/2002.
The ripening or dispersal of Calyptranthes sp. fruits was synchronous among the individuals studied, and happened during the period with the lowest precipita-tion rates, from July to October (Figure 3). During this
period, this species was the main provider of zoochoric fruits. It was observed that, upon the start of the wet sea-son, many ripe Calyptranthes sp. fruits fell, making them available to the ground foraging fauna. C. acrostichoides
dispersed from the middle of the wet season through the middle of the dry season, while M. sellowiana showed a shorter dispersal period, with great synchrony among individuals, in the wet season. Synchronical behaviour in the fruit production of a species can facilitate seed propa-gation, as it attracts more dispersing animals (Rathcke and Lacey, 1985). The period of maturation or disper-sal of A. vaccinioides fruits showed no apparent relation
to rainfall variation, this phenophase being distributed among the individuals throughout the year.
Considering all of the studied species, the circular analysis pointed out a significant tendency (Rayleigh test p < 0.001) for dispersal to occur in September (Figure 4). This result is a consequence of the higher number of
Calyptranthes sp. individuals, which presented mature or dispersed fruits at the end of the dry season and the beginning of the wet season. Nonetheless, due to the conditions of the other species throughout the year, the average vector length (r) calculated in this analysis was 0.302, a low value in a scale where 0 represents asyn-chrony and 1 represents maximum synasyn-chrony.
4. Discussion
With the exception of Miconia sellowiana, the fruit dispersal pattern observed for the studied species dur-ing the dry season is unusual. Accorddur-ing to what is de-scribed in the literature concerning tropical plants, the majority of zoochoric species have a tendency to under-go this phenophase in the wet season (Gottsberger and Silberbauer-Gottsberger, 1983; Batalha and Mantovani, 2000; Oliveira and Paula, 2001), though some studies have been performed in the transition period between the wet and dry seasons (Ferraz et al., 1999; Dalponte and Lima, 1999).
The low seasonality of the fructification event, con-sidering all studied species (r = 0.302), suggests the avail-ability of fruits throughout the year, which is necessary to maintain the mutualism between plant and disperser
(Fenner, 1998). The analysis of the average vector length (r) of each species resulted in high values, indicating syn-chrony of fructification among the individuals of each species, with the exception of Alibertia vaccinioides. The average date (µ) of this event for each species proves the dispersal of diaspores in different months, confirm-ing the event’s low seasonality when all species were considered as a group. Similar results were observed by Morellato et al. (1990) for species with fruits dispersed by animals in a montane forest. These results seem to indicate that these species respond differently to climatic variations (Fournier, 1974) or to evolutionary pressure applied by animals (Van Schaik et al., 1993).
The fruits of the studied plants are small (<10 mm diameter) and follow the pattern of little investment, pro-posed by McKey (1975), where fruits of low nutritive quality are produced in large quantities. The probable dispersers for Calyptranthes sp., Miconia sp. (Oliveira and Paula, 2001; Magalhães, 2003) and Alibertia sp. (Magalhães, 2003) are birds, which were frequently seen foraging in the area. Non-flying mammals disperse the fruits of Alibertia sp., (Oliveira and Paula, 2001; Dalponte and Lima, 1999), Miconia sp., and Coccoloba
sp. (Dalponte and Lima, 1999); and ants were detected cutting down stems and carrying fruits of Miconia sp. (Pereira and Mantovani, 2001). Feces of the tapeti rabbit,
Sivilagus brasiliensis (Lagomorpha, Mammalia), were found on some zoochoric shrubs, indicating that these animals visit the area where the fruits fall, despite their classification as browsers, and not frugivores (Emmons, 1990). Pakeman et al. (2002) observed that these animals select fruits for their diet, contributing to an increase in germination and seed dispersal. Therefore, knowledge of the displacements and fate of seeds that are carried by
Figure 3. Rainfall indexes (mm3) and frequency of
indi-viduals in fructification for four zoochoric species, during a fifteen month period, in a Canga area. Rainfall data for the years 2002-2003.
Figure 4. Complete circular representation of the number of
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animals is essential for the understanding of patterns of species establishment, community structure, and, con-sequently, for the restoration of disturbed ecosystems (Chambers, 2000). The restoration of some ecological processes, such as dispersal, may improve forest diversi-ty through external sources of fruits (Souza and Batista, 2004), which are carried through the guts of vertebrate frugivores that are attracted to recovered areas.
Miconia sellowiana was identified by Nappo et al. (2004) as the species with the best performance in coloni-zation and structuring of natural regeneration in a mined area of Minas Gerais. This secondary species dominates the classes of largest height and largest diameter. It is the main species of the superior stratum in this initial phase of natural succession. Ecological knowledge is essential during restoration processes where it is necessary to ma-nipulate an ecological system successfully to reach the desired goals (Davis and Slobodkin, 2004). When plant-animal interactions are established in a mining area, it is possible for these communities to support themselves and survive in the new environment (Frenedozo, 2004). Therefore, phenological behaviour is an important tool in degraded area recuperation programs, because it al-lows the selection of species that disperse in different pe-riods. Hence, in conclusion, the studied species showed a potential to attract animals throughout the year, and planting them for the recuperation of iron mine lands of the Quadrilátero Ferrífero may increase the communi-ties’ self-regeneration potential. By this means, self-suf-ficiency can be attained through their natural dispersers, eliminating the future need to manage fruit dispersal.
Acknowledgements — We thank the Companhia Vale do Rio Doce (CVRD) for access to the studied area, CNPq and FAPEMIG for financial support, João R. Stehmann, Ana M. Oliveira and Marcos Sobral for identification, Brenda Vartuli for field assistance, Maria Rita Scotti and Nadja M. S. Carneiro for logistics assistance, Companhia Energética de Minas Gerais (CEMIG) for meteorological information about the UHE of Peti, Eduardo Athayde for helping with the statistical analysis, Ricardo Latini for making the map, and Armando de Menezes Neto for revising the text.
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